Gametogenic Cycles of Marine Mussels, Mytilus Edulis and Mytilus Trossulus, in Cobscook Bay, Maine Aaron P
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The University of Maine DigitalCommons@UMaine Electronic Theses and Dissertations Fogler Library 12-2001 Gametogenic Cycles of Marine Mussels, Mytilus edulis and Mytilus trossulus, in Cobscook Bay, Maine Aaron P. Maloy Follow this and additional works at: http://digitalcommons.library.umaine.edu/etd Part of the Aquaculture and Fisheries Commons, and the Oceanography Commons Recommended Citation Maloy, Aaron P., "Gametogenic Cycles of Marine Mussels, Mytilus edulis and Mytilus trossulus, in Cobscook Bay, Maine" (2001). Electronic Theses and Dissertations. 146. http://digitalcommons.library.umaine.edu/etd/146 This Open-Access Thesis is brought to you for free and open access by DigitalCommons@UMaine. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of DigitalCommons@UMaine. GAMETOGENIC CYCLES OF MARINE MUSSELS, MYTIL US EDULIS AND MYTIL US TROSSUL US, IN COBSCOOK BAY, MAINE BY Aaron P. Maloy B.S. East Stroudsburg University, 1997 A THESIS Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Science (in Marine Biology) The Graduate School The University of Maine December, 2001 Advisory Committee: Bruce J. Barber, Associate Professor of Marine Sciences, Advisor Paul D. Rawson, Assistant Professor of Marine Sciences Steve R. Fegley, Professor of Marine Biology GAMETOGENIC CYCLES OF MARINE MUSSELS, MYTIL US EDULIS AND MYTIL US TROSSUL US, IN COBSCOOK BAY, MAINE By Aaron P. Maloy Thesis Advisor: Dr. Bruce J. Barber An Abstract of the Thesis Presented in Partial Fulfillment of the Requirements for the Degree of Master of Science (in Marine Biology) December, 200 1 The Mytilus edulis species complex includes three smooth-shelled blue mussels, M. edulis (Linnaeus 175 8), M trossulus (Gould 1850), and M galloprovincialis (Lamarck 1819). When any two of theses species occur sympatrically, hybridization and backcrossing of hybrid and parental genotypes is evident. Despite introgression of genes between taxa their genetic integrity is maintained. To test the hypothesis that a temporal variation in species-specific spawning times is the mechanism limiting hybridization and maintaining genetic integrity in a M edulis and M. trossulus hybrid zone in eastern Maine, mussels were sampled on monthly to semi-monthly intervals throughout 2000 from a low intertidal site in Cobscook Bay. Four polymerase-chain-reaction-based (PCR) genetic markers were used to differentiate between species. Gamete volume fraction (GVF) and oocyte area measurements indicated that both species are temporally synchronized with respect to gametogenesis and spawning. Thus low frequency of hybridization and preservation of genetic identity is not the result of temporally separated spawning times. Limited hybridization may result from gametic incompatibility, differential environmental adaptation, or selective mortality of hybrids. Preferential collection of M edulis seed for aquaculture in Cobscook Bay is thus not possible on the basis of spawning activity alone. ACKNOWLEDGEMENTS I would like to thank my advisor Bruce J. Barber for providing me with the opportunity to study at the University of Maine and for his guidance as a mentor; to my committee members Paul D. Rawson and Stephen R. Fegley, for their time and commitment to ensuring my development as a scientist; Dawna Beane for the endless preparation of histology slides; my family for their love and support in all aspects of my life, and all those who helped with the collection of animals used in my research. Special thanks to Pilar Haye for her helpful comments on my work, engaging conversations, and most of all for being a true friend in life. Funding and miscellaneous financial support of this work came from the Maine Aquaculture Innovation Center, Association of Graduate Students, and the National Shellfisheries Association. TABLE OF CONTENTS .. ACKNOWLEDGEMENTS..................................................................... ii LIST OF TABLES ................................................................................. v LIST OF FIGURES.............................................................................. vi Chapter 1. THE MYTILUS EDULIS SPECIES COMPLEX. GAMETOGENESIS. AND CULTURE 1. 1. The Mytilus edulis Species Complex ........................................... 1 1.1.1. Species Identification .................................................. 2 1.1.2. Mytilus Distributions in Eastern North America .................. 3 1.l. 3. Mytilus trossulus in Maine............................................ 4 1.1.4. The Southern Distributional Limit and Environmental Stress................................................. 5 1.2. Hybrid Zone Models and Maintenance of Genetic Identity ................6 1.3. Reproduction ...................................................................... -8 1.3.1 . Gametogenesis......................................................... 8 1.3.2. Spawning............................................................... 10 1.3.3. Assessment of Reproductive Condition ...........................11 1.3.4. Gametogenic Variation in Mytilus ................................. 12 1.4. Mussel Culture in Maine ....................................................... 13 2 . GAMETOGENIC CYCLES OF MARINE MUSSELS. MYTILUS EDULIS AND MYTILUS TROSSULUS. IN COBSCOOK BAY. MAINE Introduction..................................................................... -16 Materials and Methods ......................................................... 19 2.2.1. Site Location and Collection ........................................19 2.2.2. Genetic Characterization............................................. 19 2.2.3. Histological Preparation............................................ -20 2.2.4. Quantitative Assessment of Gametogenesis...................... 20 2.2.5 Gamete Volume Fraction (GFV) .................................. 21 2.2.6. Oocyte Area ........................................................... 21 2.2.7 Statistics............................................................... 21 Results ........................................................................... 22 Discussion...................................................................... -24 2.4.1. Biological Implications............................................ -24 2.4.2. Aquaculture Application............................................ 28 REFERENCES .................................................................................. 36 BIOGRAPHY OF THE AUTHOR ........................................................... 42 LIST OF TABLES Table 1. Relative number of males, females and undifferentiated individuals of Mytilus edulis and M. trossulus sampled throughout 2000.............................................................. .29 Table 2. Gamete Volume Fraction. Results of a three-way ANOVA testing the effect of date, species, and gender on the gametogenic cycles of Mytilus edulis and M. trossulus. ................ .30 Table 3. Mean Oocyte Area. Results of a two-way ANOVA testing the effects of date and species on the gametogenic cycles of Mytilus edulis and M. trossulus.. ............................... .31 LIST OF FIGURES Figure 1. Yearly cycle of mean (f 1 SD) gamete volume fraction for Mytilus edulis and M trossulus from Cobscook Bay, Maine. ......................................................................... .32 Figure 2a. Yearly cycle of mean (f 1 SD) gamete volume fraction for Mytilus edulis from Cobscook Bay, Maine.. ..........................33 Figure 2b. Yearly cycle of mean (f 1 SD) gamete volume fraction for Mytilus trossulus from Cobscook Bay, Maine.. ..................... .34 Figure 3. Yearly cycle of mean (+_1 SD) oocyte areas for Mytilus edulis and Mytilus trossulus from Cobscook Bay, Maine. ......................................................................... .3 5 Chapter 1 THE MYTILUS EDULIS SPECIES COMPLEX, GAMETOGENESIS, AND CULTURE 1.1. The Mytilm edulis Species Complex Common blue mussels of temperate waters of the northern and southern hemispheres make up the Mytilus edulis species complex, which is composed of M. edulis, M. galloprovincialis, and M. trossulus (Koehn 1991 ; McDonald et al. 1991 ). Of the three, M. edulis is thought to be the ancestral form from which M. galloprovincialis and M. trossulus have diverged (Stanley 1972, Seed 1992). During glaciation events of the Pleistocene, M. galloprovincialis diverged in the Mediterranean (Barsotti and Meluzzi 1968) and M. trossulus diverged in more northerly latitudes (Varvio et al. 1988). Mytilus trossulus is of Pacific origin and via trans-Arctic movement has more recently expanded its range into the Northeastern Atlantic (Vermeij 1991). Mytilus edulis presumably retained a southern rehge on the east coast and expanded north as glaciation receded, resulting in a zone of secondary contact between species. Hybridization is observed in areas where any two of the three occur sympatrically and has created reluctance to observe them as three separate species (Seed 1974, 1978; Skibinski et al. 1983; McDonald and Koehn 1988; Skibinski 1983; Skibinski and Roderick 1991 ; McDonald et al. 1991 ; Gosling 1992). Due to the expansive distribution, morphological similarities, and lack of a completely diagnostic morphological character, confusion exists over the taxonomy of the M. edulis species complex. 1.1.1. Species Identification Up to1 9 morphological characteristics have been used to distinguish among mussel species (McDonald et a1.1991; Mallet and Carver 1995; Innes